Structure, inter-annual variability, and long-term change in zooplankton communities of the Chukchi Sea

Thesis (Ph.D.) University of Alaska Fairbanks, 2016The Chukchi Sea is a complex transition zone between the Pacific and Arctic Oceans that has been experiencing dramatic change in recent decades due to shifting sea ice cover and increasing temperatures. We examine summer mesozooplankton communities of the Chukchi Sea in Alaskan and Russian waters during summers 2004, 2009, 2010 and 2012 within the scope of the RUSALCA (Russian-American Long Term Census of the Arctic) program. Community structure was highly variable between the study years, but was overall tightly correlated to water mass properties, with bottom temperature being the most significant factor influencing communities. Zooplankton biomass was dominated by the large copepod Calanus glacialis, while abundance was dominated by small shelf species of copepods, such as Pseudocalanus spp. and Oithona similis. The “cold" summers of 2009-2012 had nearly twice the biomass and abundance of zooplankton compared to the oceanographically “warm" summer of 2004. We discuss the implications of the inter-annual variability of planktonic communities within the Chukchi Sea, and the possible effects of longer-term climate change. We then look at distribution and population structure of an ecologically important species complex within the zooplankton, Pseudocalanus spp, and evaluate the implications of a warming climate for this group of copepods. While numerically dominating the communities, Pseudocalanus spp. has been historically understudied at the species level due to very subtle morphological differences between the species. Our approach used a combination of microscopic identification as well as a novel species-specific PCR identification method to discriminate between the four species found in the Chukchi Sea. Our results suggest that shifting oceanographic patterns and climate warming will have unequal impact on this group of organisms, arising from species-specific life histories and tolerance to environmental conditions. These recent observations on zooplankton are then placed into a historical context through comparison to data collected throughout the past half-century (1946-2012). Despite significant challenges associated with the highly variable spatial coverage and methodology of the available datasets, significant trends were detected. In addition to high levels of inter-annual variability, we demonstrate significant increases in zooplankton biomass and abundance in recent years compared to historical studies, as well as shifting distribution ranges for several key species. This signal was most pronounced within the copepods, particularly Calanus glacialis, which appears to be indirectly benefiting from warming of the region. While summer zooplankton communities of the Chukchi Sea have been primarily Bering-Pacific in character for as long as our records exist, continuing warming and ice loss are increasing the influence of Bering-Pacific fauna within the Chukchi region

Mock samples resolve biases in diversity estimates and quantitative interpretation of zooplankton metabarcoding data

Metabarcoding is a rapidly developing tool in marine zooplankton ecology, although most zooplankton surveys continue to rely on visual identification for monitoring purposes. We attempted to resolve some of the biases associated with metabarcoding by sequencing a 313-b.p. fragment of the COI gene in 34 “mock” samples from the North Sea which were pre-sorted to species level, with biomass and abundance estimates obtained for each species and taxonomic group. The samples were preserved either in 97% ethanol or dehydrated for 24 h in a drying oven at 65 °C (the routine way of preserving samples for dry weight measurements). The visual identification yielded a total of 59 unique holoplanktonic and 16 meroplanktonic species/taxa. Metabarcoding identified 86 holoplanktonic and 124 meroplanktonic species/taxa, which included all but 3 of the species identified visually as well as numerous species of hard-to-identify crustaceans, hydrozoan jellyfish, and larvae of benthic animals. On a sample-to-sample basis, typically 90–95% of visually registered species were recovered, but the number of false positives was also high. We demonstrate robust correlations of relative sequence abundances to relative biomass for most taxonomic groups and develop conversion factors for different taxa to account for sequencing biases. We then combine the adjusted sequencing data with a single bulk biomass measurement for the entire sample to produce a quantitative parameter akin to species biomass. When examined with multivariate statistics, this parameter, which we call BWSR (biomass-weighed sequence reads) showed very similar trends to species biomass and comparable patterns to species abundance, highlighting the potential of metabarcoding not only for biodiversity estimation and mapping of presence/absence of species but also for quantitative assessment of zooplankton communities.publishedVersio

Evidence for oscillating circadian clock genes in the copepod Calanus finmarchicus during the summer solstice in the high Arctic

The circadian clock provides a mechanism for anticipating environmental cycles and is synchronized by temporal cues such as daily light/dark cycle or photoperiod. However, the Arctic environment is characterized by several months of Midnight Sun when the sun is continuously above the horizon and where sea ice further attenuates photoperiod. To test if the oscillations of circadian clock genes remain in synchrony with subtle environmental changes, we sampled the copepod Calanus finmarchicus, a key zooplankter in the north Atlantic, to determine in situ daily circadian clock gene expression near the summer solstice at a southern (74.5° N) sea ice-free and a northern (82.5° N) sea ice-covered station. Results revealed significant oscillation of genes at both stations, indicating the persistence of the clock at this time. While copepods from the southern station showed oscillations in the daily range, those from the northern station exhibited an increase in ultradian oscillations. We suggest that in C. finmarchicus, even small daily changes of solar altitude seem to be sufficient to entrain the circadian clock and propose that at very high latitudes, in under-ice ecosystems, tidal cues may be used as an additional entrainment cue

Seasonal dynamics and life histories of three sympatric species of Pseudocalanus in two Svalbard fjords

Small copepods are the most diverse and numerous group in high-latitude zooplankton, yet our knowledge of important species remains poor because of the difficulties involved in correct species identification. In this study, we use a molecular method of identification, a species-specific polymerase chain reaction, to provide the first description of the seasonal dynamics and life histories of the important genus Pseudocalanus in two Svalbard fjords with contrasting environments. We conducted monthly investigations in the relatively warm and ice-free Adventfjorden, supplemented with seasonal samples from the colder, seasonally ice-covered Billefjorden. We found three species of Pseudocalanus (the Arctic P. acuspes and P. minutus, and the boreal P. moultoni). Pseudocalanus acuspes had a distinct annual life cycle and dominated during summer, when it actively reproduced. Surprisingly, the boreal P. moultoni was present year-round in both fjords and was the dominant species during winter; the presence of all life stages of this species throughout the year suggests a more continuous reproduction. The Arctic P. minutus was the rarest of the three species and was likely able to complete its life cycle in Billefjorden but not in Adventfjorden. Our study demonstrates that closely related species may have different life strategies and environmental preferences, which presumably make high-latitude zooplankton communities more resilient to climate change impacts on genus but not necessarily on species level

North Sea Ecosystem Cruise Report_JH2022206

The North Sea Ecosystem cruise (NSEC) is a multi-purpose survey established to monitor distribution and interactions of several components that constitute the lower trophic levels of the pelagic food web including phytoplankton, zooplankton, fish eggs and fish larvae. The cruise is managed by the IMR projects Monitoring of climate and plankton in the North Sea Skagerrak (IMR 14920) and Early life history dynamics of North Sea Fishes (IMR 14917). The cruise provides horizontal and vertical distributions of physical and chemical oceanographic parameters and phytoplankton, zooplankton fish eggs and larvae community composition and structure in the northern North Sea and Skagerrak. Since 2020 the IMR plankton survey was expanded by adding the monitoring of an additional trophic level, microzooplankton. The survey area of the North Sea Ecosystem cruise 2021 covered the northern North Sea and the Skagerrak (57-60.8ºN, 2.2ºW- 8.6ºE). Sampling were made at pre-selected stations along the IMR standard hydrographic transects.North Sea Ecosystem Cruise Report_JH2022206publishedVersio

Meroplankton Diversity, Seasonality and Life-History Traits Across the Barents Sea Polar Front Revealed by High-Throughput DNA Barcoding

In many species of marine benthic invertebrates, a planktonic larval phase plays a critical role in dispersal. Very little is known about the larval biology of most species, however, in part because species identification has historically been hindered by the microscopic size and morphological similarity among related taxa. This study aimed to determine the taxonomic composition and seasonal distribution of meroplankton in the Barents Sea, across the Polar Front. We collected meroplankton during five time points seasonally and used high-throughput DNA barcoding of individual larvae to obtain species-level information on larval seasonality. We found that meroplankton was highly diverse (72 taxa from eight phyla) and present in the Barents Sea year-round with a peak in abundance in August and November, defying the conventional wisdom that peak abundance would coincide with the spring phytoplankton bloom. Ophiuroids, bivalves, and polychaetes dominated larval abundance while gastropods and polychaetes accounted for the bulk of the taxon diversity. Community structure varied seasonally and total abundance was generally higher south of the Polar Front while taxon richness was overall greater to the north. Of the species identified, most were known inhabitants of the Barents Sea. However, the nemertean Cephalothrix iwatai and the brittle star Ophiocten gracilis were abundant in the meroplankton despite never having been previously recorded in the northern Barents Sea. The new knowledge on seasonal patterns of individual meroplanktonic species has implications for understanding environment-biotic interactions in a changing Arctic and provides a framework for early detection of potential newcomers to the system

Photoperiodism and overwintering in boreal and sub-Arctic Calanus finmarchicus populations

The copepod Calanus finmarchicus, a key species in the North Atlantic, generally spends the non-productive season by descending into deep waters and entering diapause, a physiological state characterized by reduced metabolism and arrested development. In the open ocean, overwintering depths are below 600 m, where temperature and light conditions are favourable to initiate diapause. However, C. finmarchicus has also been reported diapausing in areas with shallow water depth such as fjords, coastal waters and shelf seas. In these environments, the temperature and light conditions are different, and it has been hypothesized that under such conditions C. finmarchicus may remain active throughout winter. Here, we investigated changes in the swimming activity of C. finmarchicus from shallow fjords in the eastern North Atlantic during overwintering in response to ambient photoperiod. We conducted monthly experiments with populations from 2 fjords from different latitudes (sub-Arctic Ramfjord, 69°N and boreal Loch Etive, 56°N), measuring the locomotor activity of individual C. finmarchicus stage CVs exposed to a natural light:dark cycle. At both locations, peaks in activity in response to the light cycle were observed to shift from nocturnal during the early overwintering phase to diurnal during mid and late overwintering phase, with a minimal intensity observed during the mid-overwintering phase. In Ramfjord, activity and rhythmicity were generally lower than in Loch Etive. We conclude that C. finmarchicus remains active throughout its overwintering period when in shallow (<200 m) locations but down-regulates its locomotor activity during the main overwintering phase, which we describe as a winter resting state as distinct from classical diapause

Sea ice decline drives biogeographical shifts of key Calanus species in the central Arctic Ocean

In recent decades, the central Arctic Ocean has been experiencing dramatic decline in sea ice coverage, thickness and extent, which is expected to have a tremendous impact on all levels of Arctic marine life. Here, we analyze the regional and temporal changes in pan-Arctic distribution and population structure of the key zooplankton species Calanus glacialis and C. hyperboreus in relation to recent changes in ice conditions, based on historical (1993–1998) and recent (2007–2016) zooplankton collections and satellite-based sea ice observations. We found strong correlations between Calanus abundance/population structure and a number of sea ice parameters. These relationships were particularly strong for C. glacialis, with higher numbers being observed at locations with a lower ice concentration, a shorter distance to the ice edge, and more days of open water. Interestingly, early stages of C. hyperboreus followed the same trends, suggesting that these two species substantially overlap in their core distribution area in the Arctic Ocean. Calanus glacialis and C. hyperboreus have been historically classified as shelf versus basin species, yet we conclude that both species can inhabit a wide range of bottom depths and their distribution in the Arctic Ocean is largely shaped by sea ice dynamics. Our data suggest that the core distribution patterns of these key zooplankton are shifting northwards with retreating sea ice and changing climate conditions.publishedVersio

Sea ice decline drives biogeographical shifts of key Calanus species in the central Arctic Ocean

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Seasonal Variability in the Zooplankton Community Structure in a Sub-Arctic Fjord as Revealed by Morphological and Molecular Approaches

Phyto- and zooplankton in Arctic and sub-Arctic seas show very strong seasonal changes in diversity and biomass. Here we document the seasonal variability in the mesozooplankton community structure in a sub-Arctic fjord in Northern Norway based on monthly sampling between November 2018 and February 2020. We combined traditional morphological zooplankton identification with DNA metabarcoding of a 313 base pair fragment of the COI gene. This approach allowed us to provide the most detailed mesozooplankton species list known for this region across an entire year, including both holo- and meroplankton. The zooplankton community was dominated by small copepods throughout the sampling period both in terms of abundance and relative sequence counts. However, meroplankton was the most diverse group, especially within the phylum polychaeta. We identified four distinct periods based on the seasonal analysis of the zooplankton community composition. The pre-spring bloom period (February–March) was characterized by low abundance and biomass of zooplankton. The spring bloom (April) was characterized by the presence of Calanus young stages, cirripedia and krill eggs. The spring-summer period (May–August) was characterized by a succession of meroplankton and a relatively high abundance of copepods of the genus Calanus spp. Finally, the autumn-winter period (September–December) was characterized by a high copepod diversity and a peak in abundance of small copepods (e.g., Oithona similis, Acartia longiremis, Pseudocalanus acuspes, Pseudocalanus elongatus, Pseudocalanus moultoni, Pseudocalanus minutus). During this period, we also observed an influx of boreal warm-water species which were notably absent during the rest of the year. Both the traditional community analysis and metabarcoding were highly complementary and with a few exceptions showed similar trends in the seasonal changes of the zooplankton community structure